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The Organic Composition of Carbonaceous : The Evolutionary Story Ahead of

Sandra Pizzarello1 and Everett Shock1,2

1Department of and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604 2School of and Space Exploration, Arizona State University, Tempe, Arizona 85287-1404 Correspondence: [email protected]

Carbon-containing meteorites provide a natural sample of the extraterrestrial that occurred in the solar system ahead of ’s origin on the Earth. Analyses of 40 years have shown the organic content of these meteorites to be materials as diverse as -like macromolecules and simpler soluble compounds such as amino and polyols. Many meteoritic have identical counterpart in the biosphere and, in a primitive group of meteorites, represent the majority of their . Most of the compounds in meteorites have isotopic compositions that date their formation to presolar environments and reveal a long and active cosmochemical evolution of the biogenic elements. Whether this evolution resumed on the Earth to foster biogenesis after exogenous deliveryof meteoritic and cometary materials is not known, yet, the selective abundance of precur- sors evident in some cosmic environments and the unique L-asymmetry of some meteoritic amino acids are suggestive of their possible contribution to terrestrial molecular evolution.

INTRODUCTION that fostered biogenesis. These conditions are entirely unknown because geological and Why Meteorites are Part of the Discourse biological processes of over four billion years about the Origin of Life have long eradicated any traces of early Earth’s he studies of meteorites have long been part chemistry. On the other hand, we know that Tof investigations and discussions about the life has embarked in a long evolutionary path origin of life for the reason that some of these all through its recorded history and it seems rea- extraterrestrial bodies have reached the Earth sonable to extend to its unknown beginning the containing abundant carbon since its accretion, same evolutionary nature. Albeit a posteriori provide a natural sample of abiotic organic and without knowledge of the actual chemical chemistry, and may offer insights on the possible steps that carried this evolution, therefore, the environments and physico-chemical processes single assessment one can safely make about

Editors: David Deamer and Jack W. Szostak Additional Perspectives on The Origins of Life available at www.cshperspectives.org Copyright # 2010 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a002105 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a002105

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S. Pizzarello and E. Shock

life’s origin on the Earth is that it must have been how we still find them today, joined by icy an emergent process, through which biogenic objects from more distant locations of the solar and molecules gained the complex asso- system that were brought in by further dynam- ciative and interactive states we observe in even ical evolution of giant planets’ orbits (Levison the simplest forms of extant life. It is then easy to et al. 2009). With their crowding, hazardous see why the discourse about the origins of life orbits, and constant collisions, all of these bodies has been multidisciplinary, broad based, and put fragments on route to the Earth and have fostered many theories, all of which, with the done so through the ages. The importance of notable exception of the hypothesis meteorites for the study of prebiotic chemistry (e.g., Crick and Orgel 1973), accept the funda- is a result of this failed planet formation and not mental emergent nature of life from simple just for their obvious delivery but also because molecules. many of the belt objects never had their In exobiological (as well as astrobiological) composition drastically transformed by gravita- terms, it hasbeen proposed that life’sfundamen- tional high temperatures and pressures as larger tal evolutionary nature might have extended bodies did. Their meteoritic fragments, there- beyond its origin and might be rooted in the fore, may carry unaltered a pristine record of abioticcosmochemicalevolutionofthebiogenic early solar system chemistry as well as allow elements. C, H, N, O, P, and S are known to be the deciphering of its cosmic history. present as diverse and often complex organic The meteorites that best fit this description molecules in avarietyof extraterrestrial environ- are the carbonaceous (CCs), a prim- ments (Lazcano 2010) and their long cosmic itive subgroup of stony meteorites having an history has supported the idea of a possible exo- elemental composition that is very similar to .However,itsanalyticalbasiscomesfrom that of the Sun and the universe overall. As their the study of carbon-containing meteorites that name indicates, CCs have the distinction of con- have provided the only natural sample of chem- taining several percent amounts (1.5%–4%) ical evolution large enough for direct laboratory of carbon, which is for the most part present analyses. Uniquely, therefore, carbon containing as organic materials. These meteorites are aggre- meteorites record for us the abiotic organic gate rocks, i.e., consist mainly of a matrix made chemistry that preceded life’s origin and may as of packed together hydrous and anhydrous sili- yet reveal whether it is realistic to assume that cates that do not show signs of metamorphism these or similar materials, i.e., either by direct or alteration by high heat. However, as part of delivery or analogy of formation, might have their small planet parent bodies, CC mineralogy fostered or even inducted molecular evolution also shows that these rocks had experienced a toward biogenesis. liquid phase as well as the effects of impact shocks. For example, a recent measurement of the optical activity of three CC surfaces (Arteaga The Early Solar System, Meteorites, and the et al. 2010) showed a circular birefringence bias Possible Survival of Cosmochemical Evolution to negative values that the authors attribute The meteorites that reach the Earth are for the to chiral fractures and distortions in the clays most part fragments of , i.e., of those following mechanical forces. The meteorites’ small planetesimals that orbit the Sun in great aggregation also captured various inclusions; number between and Jupiter. By the the chondrules, to whose name CCs owe their Titius-Bode law of a regular spacing of planets classification, are round beads of glassy appear- from the Sun, their orbit should be occupied ance that have re-crystallized from a melt, i.e., by a planet; it is believed, however, that the small high heat, and bring witnesses to the variety of chunks of early solar materials reaching this area materials and processes that must have contrib- fell under the strong gravity of the already uted to CC parent bodies’ formation (Fig. 1). formed giant planets and were either scattered Overall, these meteorites do not seem to throughout or left unable to coalesce. That is differ much from terrestrial rocks, a similarity

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The Organic Composition of Carbonaceous Meteorites

obtained by X-ray microscopy of the surfaces after their exposure to selective staining with OsO4 vapors (Pearson et al. 2007). From these analyses, they appear to be broadly distributed within the matrix, intermixed with hydrous silicate components. As in other CCs, Figure 1. A CR2 meteorite stone found in the Antarctica Graves mountains (GRA 95229). The open Murchison organic materials can be broadly faces show the large chondrules that characterize this described in terms of their in aqueous family of meteorites. Chondrule and other inclusion and organic systems, a practical charac- abundance reduce the amount of matrix where terization that nevertheless leaves room for organics are found to about 30% of the geology. missed analytical targets and the possibility of unknowns (e.g., Deamer 1985). Insoluble and that has not helped their collection or preserva- soluble components represent respectively 70% tion because, if not seen to fall and promptly and 30% of total carbon and, within their mole- collected, they easily disappear in the environ- cular range, are both very complex and funda- ment. The was excep- mentally heterogeneous. tional in this respect because it fell at the very eve of lunar samples’ return in 1969 and was analyzed directly by NASA laboratories as a pos- Murchison Insoluble Organic Material (IOM) sible analog of those samples. One hundred The larger portion of Murchison organic carbon kilograms of this meteorite were recovered and is often referred to as kerogen-like because, like have been used in 40 years of analyses for prob- terrestrial , it is an insoluble macromo- ably the most comprehensive study of any extra- lecular material of complex composition that is terrestrial organic material to date. As a result of not known in much molecular detail; its average this focus, the Murchison meteorite composi- elemental abundances are C100H46N10O15S4.5. tion has long been considered representative The bulk of the IOM can be inferred only indi- not only of meteorites of the same type (Pizza- rectly from (e.g., nuclear magnetic rello et al. 2006) but, often (e.g., Luisi 2007), resonance and infrared) and by also of the capabilities of abiotic organic synthe- studies, where it is pyrolyzed by heat or oxidized ses in general. Given our yet tentative knowledge into its fragments. These analyses suggest a gen- of cosmochemical environments, it is not sur- eral structure composed of aromatic ring clus- prising that the latter assumption turned out to ters, bridged by aliphatic chains containing S, be premature and a new group of pristine mete- N, and O, with peripheral branching and func- orites found in the ice fields of Antarctica, the tional groups. By transmission electron micro- Renazzo-family of chondrites or CR, have been scopy, most of the IOM appears dispersed and offering a novel view of the possible synthetic amorphous but 10% of it is found as self- outcomes of abiotic chemical evolution as well contained nanostructures (Fig. 2), spheres as as of its prebiotic relevance. well as tubes, of diverse elemental composition that varies from close to pure graphitic C BACKGROUND (. 99%) to containing several percent amounts of O, N, and S. The IOM also contain minute The Abiotic Organic Composition of amounts of “exotic” carbon, so called because Meteorites: Prebiotic Traits and Biochemical it was likely formed in the envelopes of stars Counterparts prior to the formation of the solar system. In spite of exhaustive chemical analyses, we still On the whole, the large compositional het- have a very vague idea of where Murchison erogeneity of the IOM as well as the diversity of organic materials are actually located vis-a- its phases strongly suggest that this material is vis the inorganic components in the mete- the complex end product of cosmochemical orite. The only successful description so far was regimes and environments that varied greatly.

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Murchison Soluble Organic Compounds

The soluble organic compounds of the Murch- ison meteorite make up an abundant and diverse group of well over a thousand molecular species that vary from smaller water-soluble compounds such as amino acids and polyols 1000 nm up to 30-carbon-long nonpolar extracted only with (Table 1). As their Figure 2. Scanning electron microscope image of the large number indicates, they are also present GRA 95229 residue showing an abundance of in multiple isomeric forms up to the limit of submicron-sized spherical carbonaceous particles. their solubility. This diversity is observed thro- The particles are solid, single, and agglomerated ughout most of the various compound types with the largest close to 500 nm in diameter. The and is often a sign of their indigeneity because residue is deposited onto a carbon planchette and it contrasts starkly with the structural and func- imaged with 5 kV electrons and current of 98 pA (reprinted with express permission from Laurence tional selectivity displayed in biochemistry. It Garvie). has been analyzed in particular detail for Murchison amino acids. For example, all the possible a-amino alkylamino acids up to seven- On the other hand, in spite of being insoluble carbon were identified in Murchison extracts in acids and solvents, the IOM can free several based on the reference of synthesized standards individual compounds under conditions of high and several eight- and nine-carbon homolo- temperature and pressure similar to those of gous species could also be easily recognized terrestrial hydrothermal vents (3008C, 100 MPa) by chromatography- spectroscopy on the (Yabuta et al. 2007). These are mainly a variety basis of their spectra even if their standards of aromatic and heteroaromatic hydrocarbons were not available. Similar large abundances but also smaller noncondensed molecular spe- of N-substituted, cyclic, b-, g-, d-, and 1-amino cies and a suite of dicarboxylic acids up acids were also found and the total number of to C18 chain length. In addition, the hydrother- meteoritic amino acids can be placed at over molysis changed the IOM’s chiral response one hundred. In contrast, the whole of terres- to the Soai autocatalytic reaction in that it trial is made up of just 20 amino acids. displayed a statistical R-chiral bias prior to the Within this overall diversity, several compo- treatment but not afterwards (Kawasaki et al. nents of Murchison’s organic suite have identi- 2006), suggesting that some chiral species are cal counterparts in the biosphere. Eight of the present in Murchison IOM but cannot be meteorite amino acids are also found in pro- detected at the molecular level. These experi- teins (, alanine, proline, valine, leucine, ments show that portions of the IOM macro- isoleucine, aspartic acid, and glutamic acid) molecular structure can be modified at the and numerous other compounds are encoun- molecular level, exchange species with the solu- tered in terrestrial , as shown in ble organic pool, and possibly represent materi- Table 1. A very interesting similarity with bio- als caught in flux between aggregation states. We chemical traits was found in a group of chiral may also assume that, were meteoritic materials amino acids not present in terrestrial , exposed to hydrothermal conditions or pro- the 2-methyl 2-amino acids, which display longed exposure to water upon their fall, IOM in Murchison L-enantiomeric excesses (ee) release might have made an important contri- that, if not as large, have the same configuration bution to the organic pool of the early Earth (L-) of terrestrial protein. The ee were first when CCs delivered an estimated 1%–3% of discovered in the diastereomers of the seven- their weight in carbon during the early impact carbon 2-amino 2,3-dimethylbutaoic acid (Mautner et al. 1995). (Fig. 3) (Cronin and Pizzarello 1997) and were

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The Organic Composition of Carbonaceous Meteorites

Table 1. Classes of organic compounds in the Murchison meteorite. Compound Class Structure & Example

Carboxylic acids H3C—COOH

Amino acids NH2 Alanine – H3C–C–COOH – H

Hydroxy acids OH Lactic acid – H3C–C–COOH – H Ketoacids O Pyruvic acid – – H3C–C–H

Dicarboxylic acids H2 Succinic acid – HOOC–C–COOH

Sugar & acids OHOH Glyceric acid – – H2C–C–CHO H

Aldehydes & Ketones O – – H3C–C–H

. & H3C CH2NH2 Ethyl

Pyridine carb. acids COOH Nicotinic acid

N

Purines & NH2 N N N N H Hydrocarbons: Alyphatic H3C–CH2–CH3 Propane

Aromatic

Polar N

O O O N S COOH O Insoluble Material S N (estimated) O

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S. Pizzarello and E. Shock

COOH COOH ∗ ∗ H2N NH2 H3C NH2 ∗ ∗ (L) (L) CH3 H3C (D) 2S, 3S 2S, 3R 1.6 2R, 3R (D) m/Z 246 1.4 2R, 3S CH CH 3 3 1.2 2S3R[L] 2R3S[D] 1.0 0.8 COOH COOH 0.6 Abundance ∗ ∗ 0.4 H2N CH3 H3C NH2 ∗ ∗ 0.2 H3C CH3 0 23.0 23.5 24.0 24.5 25.0 Time (min) CH3 CH3 2S3S[L] 2R3R[D] Figure 3. and chromatographic elution of the Murchison 2-amino 2,3-dimethylbutyric acid diastereomers.

later established for the whole homologous conclusion that molecular chiral asymmetry series of these chiral compounds up to eight- preceded biochemistry. carbon long; their magnitude varies within the Nevertheless, these studies also leave many meteorite and is largest, up to 18%, for isovaline questions unanswered as to the prebiotic poten- (2-methyl-2-aminobutyric acid). As the bio- tial of an organic suite of Murchison-like com- chemical structures and functions of all life position. In fact, the large heterogeneity of today are dependent upon the exclusive chiral Murchison organic inventories and the appar- homogeneity of their , it appears ent randomness involved in their formation reasonable to assume that a , led to question the means and opportunities albeit of unknown origin, was also essential to by which such a diverse mixture of molecules, the origin and/or evolution of life. The ee of a majority of which are thermodynamically meteorites represent the only case so far of stable end products (e.g., carboxylic acids molecular asymmetry ever measured outside and hydrocarbons), could find an evolutio- the biosphere and their indigeneity is supported nary path toward the selectivity and functio- by compound specific carbon-, and nal specificity displayed by even the simplest isotopic data obtained for D-, and L-isovaline biochemistry. enantiomers (Pizzarello et al. 2003; Pizzarello and Huang 2005). Overall, the study of Murchison has dis- RECENT RESULTS closed detailed insights on the capabilities and The CR Antarctica Finds possible range of abiotic syntheses in cosmo- chemical environments. We have learned that Recorded falls of carbonaceous chondrites have this abiotic chemistry can form organic materi- been few (37 to date, since the first registered in als of considerable complexity and include 1806) and this record is needed, because these compounds similar or identical to biomole- meteorites resemble terrestrial rocks, are porous cules. Particularly captivating is the finding in nature, and quickly disappear into the envi- of chiral asymmetry in abiotic amino acids ronments if not spotted soon. For the same and, although less defined at the molecular reason, their organic analyses have also become level, the fact that some macromolecular and increasingly limited in scope with their years of inorganic phases of the meteorite show signs terrestrial residence, due to the ease with which of optical activity is intriguing as well. Con- CCs acquire biochemical contaminants. Fortu- sidered as a whole, these data support the nately, several of the meteorites recovered in

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The Organic Composition of Carbonaceous Meteorites

Antarctica are found unspoiled because of the unique shelter of the glaciers, where falling Amino acids meteorites are quickly covered by snow, remain buried within the ice, and resurface only when 2,200 the ice sheets, flowing toward the sea, encounter the obstacle of a mountain. 1,800 Renazzo family of meteorites make up a recent classification (CR) of several Antarctic “finds” that have petrology closely similar to 1000 that of the Renazzo meteorite, a CC that fell in 1 1864 and long remained unclassified. Two CR2 1000 2

meteorites (the GRA95229 and LAP02342 ) Abundances in ppm were analyzed recently for the major groups 600 of organic compounds known to be present Amines Hydrocarbons in the Murchison meteorite (Pizzarello et al. Aldehydes Carboxylic & Ketones acids 2008; Pizzarello and Holmes 2009) and have 200 shown an organic composition that differs dra- 0 matically from that of Murchison and, in fact, GRA CR2 LAP CR2 Murchison from any seen before in carbonaceous meteor- Figure 4. Comparative plot of major soluble organic ites (Fig. 4). Their organic suite is composed compound abundances in the Murchison and CR2 mainly of water-soluble compounds, between meteorites (GRA 95229 and LAP 02342 shown). which N-containing amino acids and amines are predominant. Ammonia is the single largest ee in CMs display this trait to less extent component of the suite, whereas hydrocarbons (GRA95229) or not at all (LAP02342), whereas and carboxylic acids are only minor compo- the abundance distribution of some of the nents. Novel were also the abundant distribu- meteorites’ diastereomer amino acids allowed tions found within CR2 amino acids, where the inference of an original asymmetry of their the shorter chain-length molecules of a homol- precursor aldehydes (Pizzarello et al. 2008). ogous series, e.g., glycine, alanine, and a-amino This somewhat indirect reasoning concerns isobutyric acid, are overabundant compared the diastereomers of the isoleucine to longer chain species and, in effect, account and can be explained as follows. The molecule for most of these compounds’ abundance. [2-amino3-methylpentanoic acid, CH3CH2- Several reactive compounds are found in C H(CH3)-C H(NH2)-COOH] contains two these meteorites as well, such as aldehydes, chiral centers (C) and can be present as two dif- tertiary amines, and the hydroxy amino acids ferent compounds (depending on the possible serine, threonine, allothreonine, and tyrosine distribution of the methyl branching along (Pizzarello and Holmes 2009); the latter two the alkyl chain), each with two enantiomers, groups of compounds were never detected in i.e., the pairs of D-, L-isoleucine (ile) and Murchison. D-, L-alloisoleucine (allo) (called diastereomers Another difference between CR2 and CM and shown schematically in Fig. 5B). Only meteorites is found in their respective content L-ile is present in terrestrial proteins, whereas of enantiomerically enriched chiral molecules. all four diastereomers are found in meteorites. In CR2s, the same amino acid species having A possible reaction for the formation of amino acids in meteorites is the addition of HCN to ketones and aldehydes in the presence 1The number represents a classification of petrographic type of water and ammonia (Fig. 5A) (e.g., Peltzer and estimates asteroidal secondary processes (were 2,1). and Bada 1978). Although producing an asym- 2The acronyms stand for the names of the Antarctica loca- tions where the meteorites were found: Graves mountain metric carbon in most cases (and therefore and LaPaz ice fields, respectively. a chiral molecule), this type of synthesis is

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S. Pizzarello and E. Shock

A NH ∗ 2 R CCO + NH3 + HCN R COOH H O H 2 H

B

∗ ∗

∗ ∗

∗ ∗ D-allo Mirror images L-allo HCN (RS) (SR)

H2ONH3

(S) (R) ∗ ∗

∗ ∗

Mirror images L-ile D-ile (SS) (RR)

C Abundance D-allo 182.00 Ion 153.00 7000 Ion 171.00

L-allo

5000

L-ile

D-ile 3000

1000

22.5 23.0 23.5 Time

Figure 5. Possible formative pathway of the isoleucine (ile)-alloisoleucine (allo) diastereomers in meteorites. (A) The cyanohydrine reaction. (B) Schematic of the distribution of ile and allo following the same reaction with a 2-methylbutyraldehyde precursor. (C) A chromatogram of the ile-allo diatereomers in the GRA 95229 meteorite.

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The Organic Composition of Carbonaceous Meteorites

nonstereospecific because the HCN addition were diverse and differed in both their compo- would be random and give equal amounts of sition and exposure to asymmetric effects. D- and L-enantiomers. However, the reaction results become more complex for longer The Long Cosmic History of Meteorites’ aldehydes that already contain an asymmetric Organic Materials carbon, for example, in the synthesis of the four ile and allo diastereomers from DL 2-methyl The formation of meteoritic organic com- butanal. In this case, were an ee present in pounds was actively debated after Murchison’s the aldehyde, e.g., of the (S) configuration, fall and the revelation that a large variety of those amino acids that carried the S-portion extraterrestrial organic molecules with counter- of the molecule through their synthesis (shown parts in the biosphere could be made abioti- between dotted squares in Fig. 2B) will be more cally. Clearly, to know the syntheses and locals abundant than their respective enantiomers. In responsible for their formation may have pro- the above example, this would be the (RS) allo found significance for the origin of extant life and (SS) ile compounds or, in the formalism and even a broaderexobiology. The earlier hypo- used for amino acids, D-allo and L-ile. Such theses all focused on solar system processes and, was the distribution of isoleucine diastereomers of these, the more influential were the sugges- found in the CR2 extracts (Fig. 5C) that, on the tion of possible Miller-Urey type (Miller et al. basis of the above formative premise, was inter- 1976) syntheses in small planets, following pro- preted to signify that their precursor aldehyde duction and recombination of radicals, and of enantiomers carried an original S-bias to the catalytic, FisherTropsch-type, processes in the meteorite’s parent body. early stages of the solar nebula, where carbon Overall, the compositional differences bet- monoxide could have undergone hydrogena- ween CR2- and Murchison-type meteorites tion to hydrocarbons and other compounds make stark contrasts. Where the heterogeneity (Lancet and Anders 1970). Eventually, the his- of Murchison compounds easily points to tory of the organic compounds in carbonaceous the difficulties that a primordial “soup” would meteorites was elucidated, at least in general encounter in molecular evolution, CR2 organic terms, by the stable isotope analyses of several distributions and abundances have the unques- compounds and compound classes in the tionable prebiotic appeal of being over abun- Murchison meteorite. dantly water-soluble, N-containing, and of The isotopic composition is a good indica- low molecular weight. Regardless of how CR2 tor of any molecule’s synthetic history because organic material came to be, it is also clear that the mass differences between isotopomers result an unknown combination of elemental compo- in energy differences in their bond formation sition, energetic availabilities, and cosmic con- and may to a mass dependent fractiona- tingencies made CR2 precursor environments tion, which becomes diagnostic of the physico- capable of a de facto selectivityof such “prebioti- chemical conditions affecting those reactions. cally desirable” molecular species. Ultimately, isotopic fractionation is a function Whether CR2 meteorite parent bodies would of zero point energy difference between iso- fit the new category (Levison et al. 2009) topomers (DE) and local temperature, in the of “trans-Neptunian” objects or not, certainly form: exp(-DE/T). In other words, the larger the formative environments and histories of the energy difference between isotope bonds their organic materials must have differed from and the lower the temperature, the greater the those of CMs. That the known ee-carrying potential for heavy isotope enrichment. Between amino acids as well as their ee are in lower abun- the biogenic elements, therefore, hydrogen has dance in CR2 than CM meteorites, whereas ee the potential for the most enrichment in 2H appear larger in a precursor aldehydes, would (, D) at low T, because of the high rel- seem to further allow the general inference ative mass difference of D/H isotope pair (2/1u, that abiotic organic pools in chemical evolution e.g., compared to 13C/12C ¼ 1.084). The most

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S. Pizzarello and E. Shock

dramatic demonstration of these capabilities is example, not all of Murchison amino acids fall given by the spectroscopic observations of the in the same range of deuterium enrichment, D/H ratios of molecules formed in the dense and asymmetry-carrying 2-methyl amino clouds of the where tem- acids display far larger dD values than the 2-H peratures are in the 10–30K range. Over a hun- isomers (Fig. 6). Because a similar branched dred such molecules have been described (e.g., versus linear difference in D-enrichment was Roueff and Gerin 2002), many of which show also observed between 3- and 4-amino isomers, extremely high D/H ratios. For example, the it seems reasonable to assume that branched average D/H ratio in terrestrial organic com- molecular species were processed in cold envi- pounds is approximately 1.5 1024, whereas ronments to a different degree than the linear aD/H ratio as high as 0.33 has been observed ones. On the other hand, 2-, 3- and 4-amino 13 in the interstellar molecule D2CO/DHCO acids also show different trends of C abun- (Loinard et al. 2000). dance with increasing chain lengths, which Most Murchison compounds were found decreases in the case of the 2-amino acids while enriched in D and 13C to varying degrees remains level, or even slightly increases, in the and these data, which alone suggest a relation case of the others. That is, within each level of between such molecules or their direct precur- D-enrichment, various processes of chain elon- sors and cold synthetic environments, led to a gation seem to have been possible. The obvious general theory of formation of meteorite organ- conclusion from these Murchison detailed ics that involved interstellar as well as parent analyses is that diverse cosmic regimes and syn- body processes. By this hypothesis, icy aster- thetic processes might have participated in oidal bodies accreted with abundant volatiles, producing the organic composition of this including water and deuterium-rich inter- type of meteorites. stellar organics that, upon warming and a sub- The isotopic analyses of CR meteorites ad- sequent period of aqueous phase chemistry, ded to the above scenario. The dD differences yielded the various soluble organic compounds between 2-amino acid types are still present of meteorites. and further magnified, with the two GRA95229 The possibility of parent body aqueous syn- 2-methyl amino acids analyzed showing the theses seems confirmed by the likelihood that highest dD values (þ7200‰) ever measured at least some of Murchison amino acids were for an extraterrestrial molecule by direct analy- formed via a Strecker-like reaction of precursor ses. However, d15N values determined for CR2 aldehydes and ketones, ammonia and HCN amino acids have a distribution between molec- (Fig. 5A). The evidence supporting this hypoth- ular subgroups that is opposite to the one of esis is the finding in the Murchison meteorite of their dD values, with 2-H amino acids having comparable suites of a-amino and a-hydroxy higher d15N than 2-methyl amino acids (Pizza- linear acids (although this correspondence rello and Holmes 2008). is not valid for the a-methyl compounds) and Because of the near absence of molecular of imino acids (e.g., Pizzarello and Cooper 15N values for cosmic environments3, only 2001). These are compounds in which two theoretical considerations can be offered for carboxyl-containing alkyl chains are bonded at the CR2 findings. The ones offered by Charnley the same amino group and would likely result and Rodgers (2002, 2004, 2008) describe a from a Strecker synthesis, e.g., when an amino mechanism for higher fractionations acid product becomes the reactant in place of in regions of the ISM, where the enhanced ammonia (Fig. 5). density and pressure that precede star formation However, there are isotopic as well as molec- would cause the freeze-out of most carbon- and ular trends within the Murchison organic suite that reveal significant formative distinctions 3The possibility of different stellar nucleosynthetic pathways between individual compounds and cannot for the element of nitrogen (e.g., Wannieret al. 1981) would be accounted for by any simplified model. For also further complicate their interpretation.

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The Organic Composition of Carbonaceous Meteorites

A

8000 CM2 2-H 2-aa Interstellar CM2 2-me 2-aa 7000 molecules 6000 CM2 2-H 2-aa CM2 2-me 2-aa range 5000

δ 4000 D 3000 2000 1000 0 23456 C #

B 2-H 2-amino a. 60 2-me 2-amino a. 3-amino a. 50 2-amino di-a. 40 C

13 30 δ

20 10 0 23456

C #

Figure 6. The hydrogen (A) and carbon (B) isotopic distributions of Murchison and CR2 amino acids.

containing molecules; with their dis- Very little is known of the molecular seq- appearance, the disruption of N2 formation uence of events that would have taken place in pathways in clouds of lesser density would result a prestellar core; however, we can expect that in a prevalence of gas-phase atomic nitrogen. several stages of temperature, pressure, and In turn, this would lead to the efficient pro- ensuing chemical regimes followed the initial 15 14 duction of ammonia and NH3/ NH3 ratios collapse of the presolar portion of the ISM higher than the cosmic 15N/14N ratios (to as (e.g., Ceccarelli et al. 2007). We could hypothe- much as by 80%). size, therefore, that some of the warmer stages These predictions are interesting in that of star formation might have allowed selected they appear to match, albeit in broad terms, environments, where the desorption, mixing, the findings in meteorites and the current and reactions of , precursor molecules, interpretation of meteoritic amino acid for- water, and ammonia led to the syntheses of mation. In fact, if the distinctly higher dD higher 15N amino acids and favored shorter values of 2-methyl amino acids seem to point molecular species formation. It also appears to their syntheses in cold ISM environments that such locals and the kinetic processes they and the lower values of 2-H amino acids to allow to envision could, rather than parent suggest that their syntheses took place at a later body reactions, explain some of the molecular stage in the presence of liquid water, their d15N distributions seen in the CR meteorites, such opposite trends would also fit with earlier as: the far from unity diastereomer ratios seen (ISM) and later (prestellar cores) cosmochemi- for the thermodynamically similar amino acids cal processes, albeit removed from a parent body alloile and ile (Chaban and Pizzarello 2007), environment. their erratic levels of enantiomeric excesses as

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S. Pizzarello and E. Shock

well as the preponderance of lower chain length where the (aq) indicates that the compounds species and the abundance of unreacted carbonyl of interest are all dissolved in H2O. This reaction containing molecules (Pizzarello and Holmes is not meant to depict a specific synthetic 2009). process, but instead delineates relative stabil- ities. It is evident from reaction (1) that there Abiotic Pathways to could be abundances of NH3(aq) that would favor the stability of alanine relative to propanal. Meteorites probably present just a minuscule Likewise, at strongly reduced conditions, where sample of the prebiotic potential of cosmic there may be considerable H2(aq) present, synthetic processes but, through their studies, alanine would become unstable relative to pro- we may be able to infer how common or wide- panal and NH3(aq). Quantifying the activities spread they may be. Transformations of organic (and concentrations) of NH3(aq) and H2(aq), compounds, or their synthesis from inorganic where such transformations become possible, compounds, occurs in response to thermody- can be accomplished by considering the equil- namic drives, modulated by the kinetic proper- ibrium constant for reaction (1), and manipu- ties of individual reactions. Setting aside lating its law of mass action expression. That the mechanistic details for a moment, it is useful expression, in its logarithmic form, is given by to examine how reactions may or may not be favored by the thermodynamic properties of log K ¼ log aCH CHNH COOHðaqÞ the system. Reactions involving organic com- 3 2 pounds and occurring in aqueous solution þ 2 log aH2ðaqÞ may have occurred on meteorite parent bodies, log aCH3CH2CHOðaqÞ smaller icy aggregates on their way to form asteroids or , and in selected prestellar log aNH3ðaqÞlog aH2O: (2) environments; therefore, investigating relative stabilities of aqueous organic compounds may In most dilute aqueous solutions (salinity, yield clues to these processes. This approach seawater, as a rule of thumb), it can be safely can help to answer specific questions about assumed that the activity of H2Oissocloseto1 relative abundances of organic compounds that setting it equal to 1 introduces only trivial found in carbonaceous meteorites. The follow- uncertainty. With this assumption, Equation (2) ing discussion illustrates this approach, with can be rearranged to give the specific goal of understanding the relative abundances of ammonia, amino acids, and log aNH3ðaqÞ¼2 log aH2ðaqÞlog K aldehydes.  Stabilities of amino acids relative to other aCH CH CHOðaqÞ (3) þ log 3 2 ; organic compounds during aqueous alteration aCH3CHNH2COOHðaqÞ can be assessed by considering a set of hypo- thetical overall reactions involving amino acids which represents the equation of a line on a and other aqueous organic compounds. As an plot of log aNH3(aq) log aH2(aq) with a example, the stability of alanine relative to the slope of 2 and an intercept equal to aldehyde propanal can be assessed by consider- ing a reaction in which carbon is conserved in  aCH CH CHOðaqÞ the two aqueous organic compounds, given by log K þ log 3 2 : aCH3CHNH2COOHðaqÞ

CH3CH2CHOðaqÞþH2O þ NH3ðaqÞ propanal At constant temperature and pressure, log K is a constant, which means that various lines ¼ CH CHNH COOHðaqÞþ2 H ðaqÞ; 3 2 2 can be determined based on the activity ratio alanine (1) of alanine to propanal.

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The Organic Composition of Carbonaceous Meteorites

2 2 HM HM Alanine Alanine 0 0 (aq) (aq) 3 –2 3 –2 1 1 1000 –4 –4 1000 log a NH log a NH Propanal Propanal –6 –6 0.001 0.001

–8 FMQ –8 FMQ –10 –9 –8 –7 –5–6 –4 –10 –9 –8 –7 –5–6 –4

log a H2(aq) log a H2(aq) Figure 7. Equilibrium activity diagrams showing the relative stabilities of aqueous alanine and propanal in terms of the activities of NH3(aq) and H2(aq) at (left)08C and 1 bar and (right)258C and 1 bar. Selected contours of the equilibrium ratio of activities of alanine to propanal from 1000 to 0.001 are indicated. Equilibrium constants for reaction (1) were calculated with the revised Helgeson-Kirkham-Flowers equation of state (Shock et al. 1992) using data and parameters from Shock et al. (1989); Shock and Helgeson (1990) and Shulte and Shock (1993). Also shown are activities of H2(aq) corresponding to equilibrium between hematite and magnetite (HM, reaction 4), as well as magnetite, quartz, and fayalite (FMQ, reaction 5). Thermodynamic data for come from Helgeson et al. (1978). All calculations were conducted with the software package SUPCRT92 (Johnson et al. 1992).

Plots of this type are shown in Figure 7 for Magnetite, which is one of the aqueous altera- 08C and 258C both at 1 bar, with contours of tion products identified in CI, CM, CO, CR, the activity ratio ranging from 0.001 to 1000. CV meteorites and some LL3 chondrites The bold contour labeled 1 in each plot shows (Zolensky et al. 2008) would be stable between the position of equal activities of the two the two vertical dashed lines on each plot. organic solutes at equilibrium. Ranges of rela- The presence of magnetite brackets the tive predominance of propanal and alanine are equilibrium activities of H2(aq) that could indicated, with that of alanine in each plot fall- have attained during at least a portion of the ing at higher activities of NH3(aq) and lower aqueous alteration processes occurring on activities of H2(aq), consistent with Le Chat- the Murchison parent body. If this alteration lier’s principle applied to reaction (1). Also occurred at 08C, then the equilibrium activity 25.2 shown in these diagrams are the values of log of H2(aq) fell between about 10 and 29.1 aH2(aq), at which hematite (Fe2O3) would be 10 . If, on the other hand, temperatures reduced to magnetite (Fe3O4), consistent with were warmer, these activities would change. As an example, at 258C, the equilibrium activities 24.9 28.5 of H2(aq) fall between 10 and 10 .In 3 Fe2O3 þ H2ðaqÞ¼2 Fe3O4 þ H2O; (4) dilute solutions, activities of neutral solutes cor- respond closely to concentrations (Amend and and where magnetite would be reduced to the Shock 2001). ferrous silicate fayalite (Fe2SiO4) in the presence These plots reveal the ranges of H2(aq) of quartz (SiO2) according to concentrations that are consistent with the occurrence of magnetite, and the NH3(aq) con- centrations that would provide a thermody- Fe3O4 þ H2ðaqÞþ3=2 SiO2 namic drive for the formation of an amino ¼ 3=2 Fe2SiO4 þ H2O: (5) acid rather than an aldehyde, and vice versa.

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At, for example, log a H2(aq)¼27 (equal to activity (¼1) contour in a plot like those shown about 100 nanomolar dissolved H2), conditions in Figure 7 for the presently unknown temper- in the middle of the range of magnetite stability, ature of aqueous alteration. If the amino acid 22 23 activities of NH3(aq).10 at 08C, and .10 to aldehyde ratio is a result of aqueous altera- at 258C, would favor the formation of alanine tion, then it provides us with this locus of pos- at abundances greater than those of propanal. sibilities in log a NH3(aq) versus log a H2(aq) Whether or not equilibrium is actually attained space. Likewise, ratios from GRA and Murchi- among organic compounds during aqueous son indicate that conditions during aqueous alteration events on meteorite parent bodies, alteration may have generated conditions near the persistent thermodynamic drive to form or slightly above the equal activity contour. amino acids or aldehydes depends on the If there were estimates of the activity of either chemical composition of the system. The plots H2(aq) or NH3(aq) that prevailed during in Figure 7 reveal the quantitative nature of aqueous alteration, then the equilibrium value those thermodynamic drives. They also make of the other would be uniquely defined by the it possible to begin to understand the amounts ratio of organic compounds. of NH3(aq) that would be required if amino Assuming that the relative abundances of acid concentrations were similar to aldehyde ammonia in the extracts are analogous to the concentrations or vastly different. relative abundances during aqueous alteration Comparison of the data from the CR2 mete- to the following assessment of relative orites and Murchison shown in Figure 4 indi- oxidation-reduction (redox) states during aqu- cates that the ratio of total amino acids to eous alteration events. The amino acid to alde- aldehydesþketones is on the order of 12 for hyde ratios in GRA and Murchison are about LAP and about two for GRA and Murchison. It equal, but the abundance of ammonia that can can also be seen that ammonia abundances are be extracted from GRA is much greater. There- greatest in GRA, similarly large in LAP, and fore, it seems likely that conditions during aque- very low in Murchison. These data can be com- ous alteration of the Murchison parent body binedwiththethermodynamicanalysisdepicted would plot at a lower activity of NH3(aq) than in Figure 7 in an attempt to evaluate what con- those that attained during alteration of the ditions were like during aqueous alteration, if GRA parent body. If so, then the fact that both the relative abundances of aldehydes and amino meteorites fall on about the same contour means acids were influenced by that stage of meteorite that the activity of H2(aq) was much greater history. It should be kept in mind that the data during alteration of GRA than during alteration that exist are for what is present in the meteorites of Murchison if alteration processes happened and not what may have been present in aqueous at similar temperatures on both parent bodies. solution during the alteration process. Adsorp- The abundance of ammonia in the LAP extracts tion equilibria among solutions and various is nearly as great as the GRA extracts, but the phases may differ for these two classes amino acid to aldehyde ratio is also greater. If of organic compounds, and much could have the temperature of alteration of LAP was similar happened to alter ratios inherited from such to that of GRA, then conditions during the an early stage in the history of the solar system. alteration of LAP would fall somewhat lower Let us assume that the relative abundances of in log a NH3(aq), but also considerably lower organic compounds in meteorite extracts reflects in the activity of H2(aq) to maintain the higher conditions on the parent bodies at the time the amino acid to aldehyde ratio. All else being compounds formed and that they were not radi- equal, indications are that conditions were cally reset by subsequent history. most oxidized during alteration of the Murchi- Starting with LAP, conditions consistent son parent body, most reduced during altera- with the overall amino acid to aldehyde ratio tion of GRA, and intermediate during the would fall just above and to the left of the 10 alteration of LAP. Corroborating evidence contour, which is the first above the equal may be found in the relative abundances of

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The Organic Composition of Carbonaceous Meteorites

carboxylic acids, which are more oxidized than free soluble compounds. Various molecular either amino acids or aldehydes. Redox condi- species must have interacted in the meteorites tions during alteration directly affect the poten- already prior to their fall, to a certain degree, tial for abiotic (Shock 1990; because some derivative compounds such as 1992a; Shock and Schulte 1990; 1998; Amend the carboxamides (Cooper and Cronin 1995) and Shock 1998; Shock and Canovas 2010). If are released from their extracts upon hydrolysis; the analysis outlined above survives deeper however, have been carefully searched scrutiny, the overall potential for abiotic organic for in the Murchison meteorite and not found, synthesis from inorganic starting compounds with the exception of diglycine (Shimoyama may have been greatest on the GRA parent and Ogasawara 2002). If we are trying to esti- body, despite its lower abundances of amino mate the potential of this delivery for prebiotic acids. evolution and we believe that such evolution There are several ways that these predictions had to gain some polymeric complexity for of relative redox states can be tested. One would life to ensue, then, we have to conclude that be to examine the mineralogy of the alteration the bulk of meteoritic compounds could have products in all three meteorites for evidence of provided, at best, monomeric constituents. mineral assemblages that could indicate redox In general, however, any evolutionary path has conditions that prevailed during alteration. to rely on monomeric material as well and, Another would be to seek evidence from min- just comparing with other early planetary proc- eral assemblages, associa- esses that could have led to organic compounds tions, and isotopes (oxygen in pairs or suites such as atmosphere-mediated Miller-Urey-type of minerals that formed together, for example) syntheses or the environment of hydrothermal that could bracket the temperatures of the vents, the molecular species ready-made in alteration events on each parent body so that meteorites would not appear as too bad of a quantitatively appropriate versions of the plots start. Of these, meteoritic amino acids appear in Figure 7 could be built. Also, experimental as likely candidates for further molecular evo- studies of the adsorption of ammonia, amino lution, particularly considering their selective acids, aldehydes, and other organic compounds and abundant suites found in CR2 chondrites. commonly extracted from meteorites on miner- Amino acids, the components of extant als found in meteorite alteration assemblages proteins, are able to polymerize under a variety would enable estimation of aqueous concentra- of laboratory conditions and could have done so tions or activities from the abundances of these in early Earth environments. For example, Oro’ compounds in the meteorites. and Guidry (1961) first showed that glycine readily polymerizes in the presence of ammonia Exogenous Delivery and Molecular Evolution and little water at temperatures of about 1408C. Also Leman, Orgel, and Ghadiri (2004) showed The Monomers and Their Potential that the presence of carbonyl sulfide, such as it is If we trust the record of impact craters observed found around volcanoes, could lead to easy for- in most of solar planets and satellites, meteor- mation of peptides. When of the type found ites have showered the Earth throughout geo- nonracemic in Murchison, amino acids readily logical ages and certainly did so soon after its form an activated carboxyl, e.g., as an oxazolone accretion (e.g., Chyba and Sagan 1992). Abun- by intramolecular dehydration, and polymerize dant organic materials were just as certainly conforming into helixes at lengths as short as delivered to the early Earth and, it is reasonable three-amino acid units (Crisma et al. 2004). to assume, a good portion of them survived the These findings suggest that it is plausible process. We have learned from the analyses of that exogenous amino acids acquired at least two largely different types of meteorites that some polymeric complexity during early ter- this exogenous input delivered both complex restrial evolution; it is as likely that their macromolecules of uncertain composition and overall molecular properties might have been

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S. Pizzarello and E. Shock

evolutionary factors as well. For example, all ee conditions. They have, therefore, some prebio- found so far for meteoritic amino acids have tic credibility and support the conclusion that, just one configuration, L-, whereas those whereas the extent to which meteoritic catalysts obtained for chiral molecules in natural proc- might have been effective in a mixture is enti- esses, designed experiments, or via theoretical rely unknown, their possible inductive effect schemes are all subjected to chance outcome toward chiral asymmetry in the monomeric in the absence of asymmetric influences. Simi- interactions of molecular evolution cannot be larly, several terrestrial crystals such as quartz disregarded. are chiral but their world-wide production is about equal in d- and l-forms. Also, so far, Energetic Contingencies ee have been found in amino acids that do not racemize4, meaning that their ee could Knowing that life ensued rather quickly in early have been preserved in prebiotic aqueous Earth history, it seems also realistic to assume environments. that the planet environments might have been Most importantly, amino acids as well as part of the unknown contingencies that fostered peptides are molecules with diverse catalytic the transition from abiotic chemistry to the properties that are readily displayed experimen- molecular evolution that preceded the emer- tally and in biochemistry. They can also be gence of life. If so, these environments would asymmetric catalysts, a fact suggesting that the have combined available organic compounds unique molecular asymmetry of meteoritic with favorable catalysts, which might have amino acids might have been a particularly use- been organic as well as inorganic. Just as all ful evolutionary tool. A set of experiments have known life forms have habitats, the emergence been conducted with this theme, to assess the of life may have had a habitat as well (Shock possibility that the nonracemic amino acids of et al. 1998, 2000). meteorites could have acted as catalysts during Because the record of Earth’s first geological early Earth molecular evolution and transferred erawas lost to ensuing diagenetic and metamor- their asymmetry to other prebiotic building phic changes, clays represent the first alteration blocks such as . It was found that both products of basaltic glass under hydrous condi- amino acids and can catalyze the tions and would be good candidates for aiding asymmetric aldol condensation of glycolalde- simple abiotic molecules, such as those found hyde, or and glyceraldehyde, to in meteorites, in undertaking evolutionary produce tetrose (Pizzarello and Weber 2004; steps of prebiotic significance. As detailed in Weberand Pizzarello 2006) and pentose (Pizza- Deamer and Weber (2010), these minerals are rello and Weber 2010) sugars with significant known to adsorb organic molecules and actively ee. It is interesting that these syntheses singled participate as catalysts in their syntheses and out D-erythrose and D-ribose in forming ee reactions (Williams et al. 2005). In particular, with LL dipeptides catalysts, whereas all other the smectite group of expandable clays, such sugars acquired either ee of the same configura- as montmorillonite and saponite, can undergo tion as the catalyst or, in some cases, no ee at all. surface energy changes during diagenesis that These reactions were conducted in buffered will affect their surface H-bonding at key sites water solution, made use of simple reactant and form complex aromatic and polyaromatic realistically available to the early Earth, and hydrocarbons of up to C20 from implied likely catalytic pathways under mild (e.g., Williams et al. 2005). Also, as mentioned above, conditions of very low H2O activities or elevated temperatures 4Racemization, the reversal of configurations in water, in aqueous solution can drive polymerization involves the loss and reacquisition of hydrogen by the car- reactions that involve dehydration such as pep- bon adjacent to the carboxyl group, which is slightly acidic, and is not allowed when the H at C-2 is substituted with a tide formation. The latter possibility has in- . spired several experimental investigations of the

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The Organic Composition of Carbonaceous Meteorites

potential for amino acid polymerization under of cosmochemical environments; however, they hydrothermal conditions (Shock 1992b, 1993). have not answered the basic exobiological ques- Starting with amino acids, it has repeatedly tion of whether extraterrestrial organic com- been shown that dipeptides and cyclic dipepti- pounds contributed to molecular evolution on des form rapidly in hydrothermal experiments the early Earth and to the emergence of life. (Imai et al. 1999b; Alargov et al. 2002; Li and That answer may never be possible, but, if Brill 2003; Lemke et al. 2009; Cleaves et al. we believe with Eschenmoser (2008) that life’s 2009). Occasionally, these experimental studies origin “ ...cannot be discovered, as other things also obtain small concentrations of tripeptides in science, it can only be re-invented”, meteorite and longer oligomers (Imai et al. 1999a; Tsuka- analyses will offer realistic molecular tools to hara et al. 2002), but the formation of cyclic attempt just that and much still can be done. dipeptides, which is thermodynamically fav- After forty years of studying Murchison-type ored (Shock 1992b), often dominates. It has meteorites, a new group of Antarctic finds has also been shown that if experiments are started shown that within the diverse cosmic environ- with somewhat larger oligomers, say three or ments may reside the capabilities of forming four amino acids in length, then the peptides organic suites enriched in biomolecule precur- can be lengthened by hydrothermal reactions sors and of high prebiotic appeal. The CR2 involving the monomers (Kawamura et al. organic compounds are still poorly character- 2005), and that polymers containing up to 20 ized but new studies will define their extent amino acids can be generated hydrothermally and distribution. Many small molecules that from glutamic acid or aspartic acid, which do could be useful for initiating molecular not form cyclic dipeptides (Kawamura and Shi- evolution could have escaped detection in ear- mahashi 2008). In addition, hydrothermal lier studies of these pristine meteorites and dehydration reactions involving alkanoic acids have not yet been targeted for analyses: glycolal- and glycerol produce -like molecules capa- dehyde, glyceraldehydes (detected but not ble of self-assembly (Simoneit et al. 2007). quantified or unpublished), HCN, , Taken together, these recent results show that , and small peptides are all “stuff” required condensation, polymerization, and for modeling early evolutionary biology. Hope- bond formation may commonly occur in fully, we shall know soon their distribution in hydrothermal conditions. If so, planetary proc- space also. essing of materials supplied from meteorites may have been integral to the emergence of living systems. REFERENCES

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The Organic Composition of Carbonaceous Meteorites

Pizzarello S, Weber AL. 2010. Stereoselective syntheses of Shock EL, Schulte MD. 1998. Organic synthesis during fluid pentose sugars under realistic prebiotic conditions. mixing in hydrothermal systems. J Geophys Res 103: Orig Life Evol Biosph 40: 3–10. 28513–28527. Pizzarello S, Zolensky M, Turk KA. 2003. Non racemic iso- Shock EL, Amend JP,Zolotov MYu. 2000. The early Earth vs. valine in the Murchison meteorite: chiral distribution the origin of life. In The origin of the Earth and Moon (ed. and mineral association. Geochim Cosmochim Acta 67: R Canup, K Righter), pp. 527–543. University of Arizona 1589–1595. Press. Pizzarello S, Huang Y, Alexandre MR. 2008. Molecular Shock EL, Helgeson HC, Sverjensky DA. 1989 Calculation of asymmetry in extraterrestrial chemistry: Insights from a the thermodynamic and transport properties of aqueous pristine meteorite. Proc Natl Acad Sci 105: 3700–3704. species at high pressures and temperatures: Standard Rodgers SB, Charnley SB. 2004. Interstellar partial molal properties of inorganic neutral species. recombination and nitrogen isotopic fractionation. Geochim Cosmochim Acta 53: 2157–2183. Mont Not R Astron Soc 352: 600–604. Shock EL, McCollom T,Schulte MD. 1998 The emergence of Rodgers SB, Charnley SB. 2008. Nitrogen superfractionation from within hydrothermal systems. In Ther- in dense cloud cores. Mont Not R Astron Soc 569: L48– mophiles: The keys to molecular evolution and the origin of L52. life? (ed. Adams Wiegel), pp. 59–76. Taylor & Francis, London, UK. Roueff E, Gerin M. 2003. Deuterium in molecules of the interstellar medium. Space Scie Rev 106: 61–72. Shock EL, Oelkers EH, Johnson JW, Sverjensky DA, Helgeson HC. 1992. Calculation of the thermodynamic Shimoyama A, Ogasawara R. 2002. Dipeptides and diketo- properties of aqueous species at high pressures and in the Yamato-791198 and Murchison carbo- temperatures: Effective electrostatic radii, dissociation naceous chondrites. Orig Life Evol Biosph 32: 165–179. constants, and standard partial molal properties to Shock EL. 1990. Geochemical constraints on the origin of 10008C and 5 kb. J Chem Soc, Faraday Trans 88: 803–826. organic compounds in hydrothermal systems. Origins Shulte MD, Shock EL. 1993. Aldehydes in hydrothermal sol- Life Evol Biosph 20: 331–367. utions: Standard partial molal thermodynamic proper- Shock EL. 1992a. Chemical environments in submarine ties and relative stabiirties at high-temperatures and hydrothermal systems. In: Marine hydrothermal systems pressures. Geochim Cosmochim Acta 57: 3835–3846. and the origin of life, (ed. N Holm) a special issue of Simoneit BRT, Rushdi AI, Deamer DW. 2007. Abiotic for- Origins Life Evol Biosph 22: 67–107. mation of acylglycerols under simulated hydrothermal Shock EL. 1992b. Stability of peptides in high temperature conditions and self-assembly properties of such lipid aqueous solutions. Geochim Cosmochim Acta 56: 3481– products. Adv Space Res 40: 1649–1656. 3491. Tsukahara K, Imai E-I, Honda H, Hatori K, Matsuno K. Shock EL. 1993. Hydrothermal dehydration of aqueous org- 2002. Prebiotic oligomerization on or inside lipid vesicles anic compounds. Geochim Cosmochim Acta 57: 3341– in hydrothermal environments. Origins Life Evol Biosph 3349. 32: 13–21. Shock EL, Canovas P.2010. The potential for abiotic organic Wannier PG, Linke RA, Penzias AA. 1981. Observations of synthesis and biosynthesis at seafloor hydrothermal sys- N-14N-15 in the galactic disk. Ap J 247: 522–529. tems. Geofluids (in press). Weber AL, Pizzarello S. 2006. The peptide catalyzed stereo- Shock EL, Helgeson HC. 1990. Calculation of the thermo- specific synthesis of tetroses: A possible model for dynamic and transport properties of aqueous species at prebiotic molecular evolution. Proc Natl Acad Sci 103: high pressures and temperatures: Standard partial molal 12713–12717. properties of organic species. Geochim Cosmochim Acta Yabuta H, Wiliams LB, Cody GD, Alexander CMO’D, 54: 915–945. Pizzarello S. 2007. The insoluble carbonaceous material Shock EL, Schulte MD. 1990. Amino acid synthesis in carbo- of CM chondrites: A possible source of discrete organic naceous meteorites by aqueous alteration of polycyclic compounds under hydrothermal conditions. Meteor aromatic hydrocarbons. Nature 343: 728–731. Planet Sci 42: 37–48.

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The Organic Composition of Carbonaceous Meteorites: The Evolutionary Story Ahead of Biochemistry

Sandra Pizzarello and Everett Shock

Cold Spring Harb Perspect Biol 2010; doi: 10.1101/cshperspect.a002105

Subject Collection The Origins of Life

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